On the Identification of Key Intermediates During the NO and H2S

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Article

On the Identification of Key Intermediates During the NO and HS Crosstalk Signaling Pathways 2

Mohamed Cheraki, Muneerah Mogren Al-Mogren, Gilberte Chambaud, Joseph S. Francisco, and Majdi Hochlaf J. Phys. Chem. A, Just Accepted Manuscript • DOI: 10.1021/acs.jpca.7b11821 • Publication Date (Web): 28 Feb 2018 Downloaded from http://pubs.acs.org on March 2, 2018

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The Journal of Physical Chemistry

On the Identification of Key intermediates During the NO and H2S Crosstalk Signaling Pathways

Mohamed Cheraki,$ Muneerah Mogren Al-Mogren,£ Gilberte Chambaud,$ Joseph S. Francisco,# and Majdi Hochlaf$, * $

Université Paris-Est, Laboratoire Modélisation et Simulation Multi Echelle, MSME UMR 8208 CNRS, 5 bd Descartes, 77454 Marne-la-Vallée, France

£

Chemistry Department, Faculty of Science, King Saud University, PO Box 2455, Riyadh 11451, Kingdom of Saudi Arabia

#

Department of Chemistry, University of Nebraska-Lincoln. 433 Hamilton Hall, Lincoln, NE 685880304, USA

1

ACS Paragon Plus Environment

The Journal of Physical Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Abstract The stable isomers and electronic states of [S,S,N,O]- species are investigated with a special focus on the most relevant isomers that could be involved in the NO/H2S cross-talk pathways in biological media. This work identifies eight stable anions, among which are the already known cisSSNO- and trans-SSNO- molecules and a new NO3--like anionic species, NS2O-. Our computations show that the previously determined structure in lab experiment is trans-SSNO-, which is not relevant for biological activity in vivo. Instead, NS2O- is proposed as the most likely key intermediate in vivo during important biological processes. This result alleviates the corresponding controversy in the literature.

2


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I.

Introduction In 1998, the Nobel Prize in Medicine was awarded to Furchgott, Ignarro and Murad for their

discoveries regarding the function of nitric oxide, NO, as a signaling molecule in the cardiovascular system. Prior to that, NO was voted by scientists as the molecule of the year in 1992 1 because this small molecule is the first gaseous compound found to act as a chemical neurotransmitter. Since then, this molecule has been established to serve as biological regulator and as cellular signaling molecule by influencing and controlling a wide range of essential bodily functions (cardiovascular, nervous and immune) and physiological and pathological processes. NO is also known to interact with both antiand prooxidants in plant cells,2 where its bioavailability and homeostasis are controlled by Snitrosobased enzymes (e.g., S-nitrosoglutathione reductase). On the other hand, NO regulates antioxidant enzymes: There is interplay between NO and reactive oxygen species (ROS) in response to stress.2 In addition to NO, two other gaseous endogenous molecules are now identified as vital signaling molecules, namely, carbon monoxide, CO,3 and hydrogen sulfide, H2S.4,5 These compounds play crucial roles in post conditioning-induced cardioprotection, in blood pressure regulation and in the regulation of protein cysteine residue activity (e.g., S-sulfhydration and S-nitrosylation). Hence, they affect the activities of biological entities. Moreover, CO and H2S are closely connected to the modulation of nitric oxide signaling pathways in the body and in plants.6 Thus, the corresponding pathways are surely overlapping and complex. Several mechanistic aspects of the implications of these small molecules still need to be characterized and treated in depth. Among the identified key molecular species are exotic endogenous molecules such as thionitrous acid (HSNO 7), peroxynitrite (OONO(SSNO

- 11,6

8-10

) and nitrosopersulfide anion / perthionitrite

). Whereas the role and biological origin of OONO-

those of HNSO and SSNO are still subject to controversy.

6,11

8-10,12

are relatively well understood,

This controversy also concerns their

potent key role in the cross-talk signaling pathways. To explain the enhancement in fluorescence during the heme-iron-catalyzed reduction of nitrites in the presence of H2S, Filipovic and coworkers7,13 proposed the existence of HSNO under physiological conditions and provided a mechanism for its formation and action in vivo. Some of the theoretical and experimental works carried out after their discovery corroborate these findings.14-16 In contrast, Cortese-Krott et al.17,18 and Bianco and Fukuto19 showed that the bioactive reaction products of the NO/H2S interaction are S/Nhybrid species, polysulfides, and nitroxyl with emphasis on the SSNO- anion. Subsequently, several experimental and theoretical studies20-22 have supported this hypothesis. Meanwhile, Filipovic and coworkers23 have expressed some doubts about the implication of SSNO- in the sustained bioactivity of NO. The key intermediate during this cross-talk pathway is still not identified because of the lack of information on small molecular systems that might be involved in the process, including HSNO and SSNO-. Nevertheless, previous investigations have showed that NO-releasing molecules should 3



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possess (i) small dissociation energies in their ground states or (ii) repulsive electronic states along the NO-releasing coordinates if they are induced by UV-Vis photon absorption and (iii) long-lived electronic states in the Vis domain that may serve as intermediates/precursors for fluorescence. In addition, this key intermediate molecular species is that may explain the observed in vivo absorbance at ~412 nm. State-of-the-art theoretical computations are performed on the stable forms and the energetics (electron affinities (EAs) and dissociation energies) of the [S,S,N,O] anionic system in its ground and excited electronic states. These species are characterized spectroscopically, and these data are compared to the measured bands in laboratory experiments and in vivo. Thus, we strongly support the key role of SSNO- and identify the corresponding intermediate isomer.

II.

Computational Section In this study, all calculations were performed using the MOLPRO 2015 package.24 We started

by looking for minima on the singlet potential energy surface (PES). Harmonic frequencies were also computed and adiabatic electron affinities were deduced. These stable geometries (all positive frequencies) were obtained by studying the attachment of an electron on the 10 stable structures for the neutral [O,N,S,S] molecular system computed by Ayari et al.25 The methods we used are coupled clusters with perturbative treatment of triple excitations ((R)CCSD(T))26,27 and the explicitly correlated version ((R)CCSD(T)-F12).28,30 Prior to that, the monoconfigurational nature of the wavefunctions of the ground states of the [O,N,S,S]- system has been checked using Complete Active Space SelfConsistent Field (CASSCF)31,32 method. For (R)CCSD(T) computations, the basis sets used are the aug-cc-pV(X+d)Z (X=D,T,Q)33-35 which take into account the tight-d functions allowing for a better 36,37

description of sulfur containing molecules as established in Refs. 38

the atoms were described using the cc-pVXZ-F12 (X=D,T)

When using (R)CCSD(T)-F12,

basis sets in conjunction with the

MOLPRO default choices for the density fitting and resolution of identity basis sets. Afterwards, we extrapolated the energies and the geometrical parameters to the complete basis set (CBS) limit using the two- parameter equation 39 = +

where X is the cardinal of the basis set; A is a fitting parameter and YCBS is the extrapolated quantity. In Ref. 40, a wide discussion is given in the validity of this procedure to get accurate energetic and structural parameters. The full set of the results are given in Figure S1 and Tables S1-S3. They correspond to the equilibrium geometries, vibrational frequencies, electron affinities, relative energies and dissociation energies to form atom + triatom and diatom + diatom fragments. Generally, the (R)CCSD(T)-F12/CBS data and those obtained using (R)CCSD(T)/CBS method are very close. For

4


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instance, differences in bond lengths and in angles do not exceed hundredths of Bohrs and tenths of degrees, respectively. In order to study the excited states of the [O,N,S,S]- system, we used the internally contracted multi reference configuration interaction (MRCI)41-43 and newly implemented explicitly correlated version (MRCI-F12) methods,44-46 on top of CASSCF calculations. At CASSCF, the active space we have used is the full valence where the three lowest valence molecular orbitals were kept doubly occupied. In MRCI calculations, we considered all configurations of the CI expansion of the CASSCF wavefunctions as a reference. We started by computing 8 (4 respectively) electronic states for the isomers belonging to the point group (respectively point group). From this preliminarily result, we selected the states which were located below the corresponding neutral parent state and restarted the computations. Indeed, our methodology did not allow correctly describing the electronic states located above their corresponding neutral parent.

III.

Results and Discussion

cis-OSNS-

trans-OSNS-

cis-OSSN-

trans-OSSN-

cis-SSNO-

trans-SSNO-

cyc-SSNO-

NS2O5



Figure 1: Optimized stable forms of the OSNS-, OSSN-, SSNO- and NS2O- anions and their geometrical parameters, as computed at the CCSD(T)-F12/CBS level. Distances are in bohrs (1 bohr = 0.520 Å) and angles are in degrees. Electron affinities (EA, in eV) are also given. See the Supporting Information for more details.

Figure 1 displays the stable forms of the [S,S,N,O] anion. The full set of their geometric parameters, harmonic frequencies, relative energies and EAs, as computed at the CCSD(T)/aug-ccpV(X+d)Z (X=D,T,Q,CBS) and CCSD(T)-F12/cc-pVXZ-F12 (X=D,T,CBS) levels, is listed in Table S1 of the Supporting Information. Eight forms are obtained, whereas the neutral system possesses ten isomers (electron attachment to C1-SSNO and C1-OSSN neutrals leads to unstable species).25 The anionic structures obtained belong to OSNS-, OSSN- and SSNO- groups of molecules. OSNS- has two isomers, namely, cis-OSNS- and trans-OSNS-, which are planar chain-type molecules (Cs point group). OSSN- also presents both cis- and trans-isomers that belong to the Cs point group. For SSNO-, four different isomers are found, namely, cis-SSNO- and trans-SSNO-, which are also planar chaintype species (Cs point group); cyc-SSNO-, which is a pyramidal structure; and finally NS2O-, which is a NO3--like molecule and hence belongs to the C2v point group. Note that only cis- and trans-SSNOand cyc-SSNO- were already known. As stated above, this may account for the lack of full identification of SSNO- species in vivo. Compared to their neutral parent [S,S,N,O] species,25 the external NS bonds in cis-OSNS- and trans-OSNS- are notably longer by ~0.2 Bohr. Considering the frontier molecular orbitals (MOs) of these species, as given in Ref. 25, this result can be explained by the addition of an extra electron when forming the anion to the anti-bonding character of their singly occupied molecular orbital (SOMO), which is mainly located in this NS bond. For cis-OSSN- and trans-OSSN-, the central SS bond length is longer in the corresponding neutral species by ~0.5-0.6 Bohr. Here, the SOMO has a bonding character. Thus, adding an electron to this MO will shorten the bond. With cyc-SSNO-, the ON bond length is longer in the anionic species by ~0.6 Bohr for the same reason as the OSNS- isomers. For the cis- and trans-SSNO- isomers, there is a shortening of the central NS bond upon adding an electron to neutral cis- and trans-SSNO. Finally, it should be noted that the NS2O- anion and the NS2O neutral species possess essentially the same bond lengths with a difference of less than ~0.1 Bohr between the two species. This can be explained by the concentration of their SOMOs on the lone pairs of the sulfur atoms. All of the eight anionic molecules present relatively large EAs (> 2 eV, Figure 1). Such large EAs are known only for very few molecular species, such as NO3,47 carbon chains Cn and CnH 48,49 and CnN

49

compounds. In particular, the newly identified NS2O species has an EA greater than 3 eV

similar to NO3 (EA(NO3) = 3.937 eV 47). Such large EAs may allow stable excited states of the anionic systems to exist. 6


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Table 1: (R)CCSD(T)/CBS dissociation energies (D0, in eV) from the tetratomic [O,N,S,S]- isomers to form atomic+triatomic and diatomic+diatomic fragments. See Tables S2 and S3 of the Supplementary material for more details. We give also the dissociation energies for the neutral species as given in Ref. 25. Reaction

D0

Reaction

cis-OSNS- → O (3P) + SNS- (11A′)

5.00

cis-OSSN → O(3P)+SSN(12A′)

-

- 2

-

3

cis-OSNS → O ( P) + SNS (1²A′) -

1

5.62

D0

3

2

trans-OSSN → O( P)+SSN(1 A′) 3

2

4.48 3.78

cis-OSNS → S ( P) + NSO (1 A′)

2.90

cis-SSNO → S( P)+SNO(1 A′)

3.75

cis-OSNS- → S- (2P) + NSO (1²A′)

3.99

trans-SSNO → S(3P)+SNO(12A′)

1.30

-

3

-

1

3

2

trans-OSNS → O ( P) + SNS (1 A′)

4.79

C1-SSNO → S( P)+SNO(1 A′)

2.78

trans-OSNS- → O- (2P) + SNS (1²A′)

5.42

cyc-SSNO → S(3P)+SNO(12A′)

2.59

-

3

-

1

3

2

trans-OSNS → S ( P) + NSO (1 A′)

2.70

C1-OSSN → O( P)+SSN(1 A′)

2.46

trans-OSNS- → S- (2P) + NSO (1²A′)

3.80

cis-OSNS → O(3P)+SNS(12A′)

4.31

-

3

-

1

-

- 2

cis-SSNO → O ( P) + SSN (1²A′)

5.57

cis-SSNO- → S (3P) + SNO- (11A′)

3.26

cis-SSNO → O ( P) + SSN (1 A′)

-

3.96

- 2

cis-SSNO → S ( P) + SNO (1²A′)

3.40

trans-SSNO- → O (3P) + SSN- (11A′)

3.75

-

- 2

-

3

-

- 2

trans-SSNO → O ( P) + SSN (1²A′) -

1

trans-SSNO → S ( P) + SNO (1 A′) trans-SSNO → S ( P) + SNO (1²A′) -

3

-

1

5.11

cis-OSSN → N ( S) + SSO (1²A′)

2.62

trans-OSSN- → O (3P) + SSN- (11A′)

3.40

-

- 2

-

4

trans-OSSN → O ( P) + SSN (1²A′) -

2.52

cyc-SSNO- → S (3P) + NSO- (11A′)

0.36

- 2

cyc-SSNO → S ( P) + NSO (1²A′)

1.46

cyc-SSNO- → S (3P) + cyc-SNO- (11A′)

4.08

-

- 2

cyc-SSNO → S ( P) + cyc-SNO (1²A′)

3.11

NS2O- → O (3P) + SNS- (11A′)

3.65

-

- 2

-

3

NS2O → O ( P) + SNS (1²A′) -

1

2.48

5.01

trans-OSSN → N ( S) + SSO (1²A′) -

NS2O → O( P)+SNS(1 A′)

3.18

cis-OSSN- → O- (2P) + SSN (1²A′) -

4.11

trans-OSNS → O( P)+SNS(1 A′)

3.05

3.49

4

2

5.37

cis-OSSN → O ( P) + SSN (1 A′) -

3

4.27

NS2O → S ( P) + SNO (1 A′)

2.63

NS2O- → S- (2P) + SNO (1²A′)

2.76 7


3

2


NS2O- → S (3P) + cyc-SNO- (11A′) -

- 2

5.27

NS2O → S ( P) + cyc-SNO (1²A′)

4.30

cis-OSNS- → NS (X2Π) + OS- (X2Π)

3.23

-

-

3 -

3 -

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cis-OSNS → SO(X3Σ−) + SN(X2Π) 3 −

2

cis-OSNS → NS (X Σ ) + OS (X Σ )

3.17 trans-OSNS → SO(X Σ ) + SN(X Π)

trans-OSNS- → NS (X2Π) + OS- (X2Π)

3.03

-

-

3 -

cis-SSNO → S2(X3Σg-) + NO(X2Π)

3 -

3

trans-OSNS → NS (X Σ ) + OS (X Σ ) 2.97 trans-SSNO → S2(X cis-SSNO- → S2- (X2Πg) + NO (X2Π) -

-

2

2

trans-SSNO → S2 (X Πg) + NO (X Π) -

2

-

2

1.24 1.03

Σg-)

2

+ NO(X Π)

C1-SSNO → S2(X3Σg-) + NO(X2Π) 3

-

2

cyc-SSNO → S2(X Σg ) + NO(X Π 3 -

2

1.94 1.74 0.50 0.21 0.18 -1.05

cis-OSSN → NS (X Π) + OS (X Π)

2.05

C1-OSSN → SO(X Σ ) + SN(X Π)

1.43

cis-OSSN- → NS- (X3Σ-) + OS (X3Σ-)

1.97

cis-OSSN → SO(X3Σ-) + SN(X2Π)

0.71

-

2

-

2

3 -

2

trans-OSSN → NS (X Π) + OS (X Π)

1.95

trans-OSSN → SO(X Σ ) + SN(X Π)

0.67

trans-OSSN- → NS- (X3Σ) + OS (X3Σ)

1.87

NS2O → SO(X3Σ-) + SN(X2Π)

0.24

-

-

2

2

NS2O → S2 (X Πg) + NO (X Π)

0.61

Table 1 presents the dissociation energies of the [S,S,N,O]- anions to form the atom+triatom and diatom+diatom fragments. For the dissociations leading to triatomic and atomic fragments, the energies are relatively high, ranging from 2.5 to 5 eV, with the exception of cyc-SSNO-, which possesses a D0 of ~1 eV for S/S- loss. These D0’s are in line with the breaking of relatively strong external bonds in [S,S,N,O]-. Also these dissociation energies are relatively larger than those of the corresponding neutral species because of the reinforcement of the bounding character of these molecular orbitals by adding an electron. For instance, we compute dissociation energies of 3.75 eV and 5.37 eV for trans-SSNO- → O (3P) + SSN- (11A′) and trans-SSNO- → O- (2P) + SSN (1²A′), respectively, whereas the breaking of the NO bond in neutral trans-SSNO (→ S(3P)+SNO(12A′)) requires much less energy (D0 ~ 1.30 eV). For the formation of diatomic + diatomic fragments from the corresponding tetratomic molecules, all dissociation energies are positive in the range from 0.5 to 2 eV, with the exception of cis-OSNS- and trans-OSNS-, which have a central SN bond dissociation energy of approximately 3 eV. Again, Table 1 shows that these dissociation energies are larger for the anions than for the neutrals due to the strengthening of the bonding character of the central bonds by adding an extra electron to their SUMOs. Interestingly, the biologically relevant SSNO- isomers possess the weakest central bonds. For instance, the D0 values are computed to be approximately 1.2, 1.0 and 0.6 eV for cis-SSNO-, trans-SSNO- and NS2O-, respectively. Their dissociation would simply involve breaking SN bonds to give NO and S2-, as NO has a weak EA (EA(NO) = 0.026 eV 50). Thus, NS2O- exhibits the lowest dissociation energy, enabling easy release of NO. Compared to the HNSO molecule, the central bond dissociation energy is evaluated at 1.08-1.26 eV, 14,51 which is close to those 8


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of cis- and trans-SSNO- but remains larger than that of NS2O-. Hence, NS2O- better fulfils condition (i) for NO release provided above. Table S4 lists the pattern of the electronic states of the different isomers using the MRCI and MRCI-F12 levels of theory in conjunction with the aug-cc-pV(X+d)Z (X=D,T,Q) or cc-pVXZ-F12 (X=D,T) basis sets, respectively. In this table, only the anionic [O,N,S,S]- electronic states located below the corresponding neutral molecule (excitation energy lower than the respective EA) are presented. Since MRCI and MRCI-F12 generally provide similar data, we will refer to those from MRCI-F12/aug-cc-pVTZ below. Because of the large EAs of these molecules, they all present one or two excited states, except for cyc-SSNO-, for which no electronic states are found. For all these species, the excitation energies are computed in the 1.9-3.1 eV energy domain, which is in the visible region. Nevertheless, based on the energetics discussed above, the species OSNS-, OSSN- and of cycSSNO- can be excluded from involvement in biological phenomena. Table 2: MRCI-F12/aug-cc-pVTZ vertical excitation energies (E, in eV) of cis- and trans-SSNO- and of NS2O-. Reference energy is the energy of the corresponding ground state at equilibrium. The corresponding wavelengths with (λsol, in nm) and without (λ, in nm) considering solvent effects are also given. cis-SSNO-

trans-SSNO-

NS2O-

1A′

11A″

1A′

11A″

21A′

1A1

11A2 [b]

11B2 [c]

E

0.00

2.55

0.00

2.27

2.81

0.00

2.05

3.18

λ

-

486

-

546

441

-

604

390

λsol [a]

-

~495

-

~555

~450

-

~615

~400

~412

λ from in vivo exp.

[d]

~550 & ~428 [e] ~448 [f]

λ from lab exp. d)

~446 [g] a. Solvent effects are estimated to induce ~10 nm shifts in the bands based on the works on NO3-. See Ref. 54 for more details. b. The 1A1 11A2 transition is not allowed. Thus the lifetime of this state is long. c. The lifetime of this electronic state is estimated 74.1 ns at the MRCI-F12/aug-cc-pVTZ level. d. Ref. 18. e. Ref. 23. f. Ref. 53. g. Ref. 52.

9



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Table 2 gives the vertical excitation energies of cis- and trans-SSNO- and of NS2O- as computed at the MRCI-F12/aug-cc-pVTZ level. We also used the MRCI-F12 wavefunctions to evaluate the transition dipole moment (Re) between the 11B2 and 1A1 states of NS2O-. We compute Re = -4.206 Debye. Re is used to deduce the radiative lifetime (τ in s) of this electronic state using the following formula τ = 6.07706 x 10-6 1/( |Re|2 ν3)

where ν (in eV) is the corresponding MRCI-F12 transition energy. The result is given in Table 2. According to the data given in Table 2, trans-SSNO- is most likely formed after mixing S + PNP+NO2- in Ref.

23

, and the isolated persulfides react with nitrite.

52

The measured absorption

spectrum consists of two bands at ~428 and ~550 nm, which may be associated with those computed here at ~450 nm and 555 nm for trans-SSNO- isomer. For the first band, there is better agreement with the band measured in 1985 at 448 nm by Seel et al. 53 and more recently at ~446 nm by Bailey et al. 52 Thus, this good agreement between the computed and the measured band energies for trans-SSNOconfirms the detection of this isomer in laboratory experiments. Nevertheless, none of the computed bands correspond with those measured in lab and in vivo experiments. This renders questionable the assignment of these bands to the cis-SSNO- isomer as stated by Filipovic and co-workers in Ref. 23.

Figure 2: MRCI-F12/aug-cc-pVTZ one-dimensional evolution of the potentials of the lowest electronic states of cis-SSNO- (in A), trans-SSNO- (in B) and NS2O- (in C and D) along the dR 10


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parameter. We give also those of the lowest electronic states for the neutral NS2O (dashed curves). dR corresponds to the variations with respect to the equilibrium geometry defined in each cut. The reference energy is the energy of the NO(X2Π) + S2-(X2Π) asymptote. In A/B, the angles are fixed at ONS = 119.4°/113.8° and NSS = 113.8°/108.7°. In C, the SNO angles are set to 119.9°. In D, the SS and NO distances are fixed at their respective diatomic ground state equilibrium values (RSS = 3.570 Bohr and RNO = 2.175 Bohr) and R = 1.911 Bohr when computing the neutral. For the anion, the SS distance is fixed at 3.789 Bohr, RNO = 2.175 Bohr and R = 1.599 Bohr. SS* corresponds to S2(a1∆g). Figure 2 presents the one-dimensional cuts of the 6D potential energy surfaces of the lowest singlet states of cis-SSNO-, trans-SSNO- and NS2O- as computed at the MRCI-F12/aug-cc-pVTZ level. They are the probable candidates for releasing NO in vivo. This figure shows that both cis- and trans-SSNO- isomers have bound ground states but repulsive excited states. This is consistent with the decomposition of trans-SSNO- in the presence of visible light observed in the experiments of Filipovic and co-workers.

24

In contrast, NS2O- has bound ground and electronic excited states. Thus, only

NS2O- has long-lived excited electronic states that may fluoresce. This definitely excludes the implication of cis- and trans-SSNO- in biological processes since they cannot explain the experimentally observed fluorescence bands. However, NS2O- does have long-lived excited electronic states. Indeed, this anionic form fulfils the requirements stated by Filipovic and co-workers in Ref.23 and are fully consistent with the in vivo experimental observations of Cortese-Krott et al.17,18 and of Bianco and Fukuto.19 As stated above, this species possesses a low dissociation energy towards NO release. NS2O- is also the species that allow assigning the observed in vivo absorbance band at ~412 nm.

18

This band corresponds to the population of the second excited state of NS2O- (at λ ~400 nm

after considering solvent-induced effects, Table 2). Additionally, note that the S0-S1 transition is forbidden for NS2O-; thus, NS2O- spectrum should feature a unique band, as observed experimentally. This confers also a long-lived character for the S1 state of this species. Moreover, Figure 2D shows that the shapes of the electronic excited states of NS2O- evolve from bound to repulsive when the SS distance is varied. This is in line with the easy release of NO after photoexcitation where large amplitude motions are expected. We also find a local minimum on the ground potential when SS distance is fixed to its value in S2-(X2Πg)). This local minimum may play a role during these biochemical processes. In conclusion, it can be asserted that NS2O- is most likely the key intermediate in the NO and H2S cross-talk signaling pathways. IV.

Conclusions After benchmarks on the structural, spectroscopic and electronic states of [O,N,S,S]- molecular

species and their comparison to in vivo and laboratory observation, we propose NS2O- C2v form as a key intermediate in the NO and H2S cross-talking signaling pathways in biological media. The present 11



work provides all necessary structural and spectroscopic (vibrational and electronic) parameters that may be used for the identification of NS2O- anion in laboratory. Synthesis and characterization of exotic biochemical molecular systems represents an active field in physical chemistry and inorganic chemistry, where new routes are undertaken.

16,55

Also our work should motivate the reinvestigation

of in vivo experiments in order to elucidate the central role of NS2O- in NO and H2S biochemistries.

ASSOCIATED CONTENT Supporting Information

The Supporting Information is available free of charge on the ACS Publications website at XX. Details of the computational methodologies and the full set of data are given.

AUTHOR INFORMATION Corresponding Authors *E-mail: [email protected] (M.H.). ORCID M. Hochlaf: 0000-0002-4737-7978 J. S. Francisco: 0000-0002-5461-1486

Notes The authors declare no competing financial interest.

ACKNOWLEDGMENTS The authors extend their appreciation to the International Scientific Partnership Program (ISPP) at King Saud University for funding this research work through ISPP# 0045. We gratefully acknowledge the support of the COST Action CM1405 entitled MOLIM: Molecules in Motion.

REFERENCES (1) Koshland Jr., D. E. The molecule of the year. Science 1992, 258, 1861. (2) Groß, F.; Durner, J. ; Gaupels, F. Nitric oxide, antioxidants and prooxidants in plant defense responses. Front. Plant. Sci. 2013, 4, 419. (3) Peers C. C.; Steele, D. S. Carbon monoxide: A vital signalling molecule and potent toxin in the myocardium. J. Mol. Cell Cardiol. 2012, 52, 359. (4) Paul B. D.; Snyder S. H. H2S: A novel gasotransmitter that signals by sulfhydration. Trends in Biochemical Sciences 2015, 40, 687. (5) Paul B. D.; Snyder S. H. H2S signalling through protein sulfhydration and beyond. Nature Rev. Mol. Cell Biology 2012, 13, 499. 12


Page 12 of 17

Page 13 of 17 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(6) Signaling and communication in plants 2016. Gasotransmitters in Plants. The rise of a new paradigm in cell signaling. Editors: Lorenzo Lamattina, Carlos García-Mata. ISBN: 978-3-31940711-1 (Print) 978-3-319-40713-5. (7) Filipovic, M. R.; Miljkovic, J. L.; Nauser, T.; Royzen, M.; Klos, K.; Shubina, T.; Koppenol, W. H.; Lippard, S. J.; Ivanović-Burmazović, I. Chemical characterization of the smallest Snitrosothiol, HSNO: Cellular cross-talk of H2S and S-nitrosothiols. J. Am. Chem. Soc. 2012, 134, 12016. (8) Pacher, P.; Beckman, J. S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiological Reviews 2007, 87, 315. (9) Szabó, C.; Ischiropoulos, H.; Radi, R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nature Reviews Drug Discovery 2007, 6, 662. (10) Beckman, J. S.; Koppenol, W. H. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and the ugly. Am J Physiol Cell Physiol. 1996, 271, C1424. (11) Bari, S. E.; Olabe, J. A. Chapter: New features of the NO/H2S cross talk: A chemical basis. Gasotransmitters in plants. Part of the series signaling and communication in plants pp 289-327 (2016). (12) Jia, X.; Chen, Q.; Yang, Y.; Tang, Y.; Wang, R.; Xu, Y.; Zhu, W.; Qian, X. FRET-based mitospecific fluorescent probe for ratiometric detection and imaging of endogenous peroxynitrite: Dyad of Cy3 and Cy5. J. Am. Chem. Soc., 2016, 138, 10778. (13) Miljkovic, J. L.; Kenkel, I.; Ivanović-Burmazović, I.; Filipovic, M. R. Generation of HNO and HSNO from nitrite by heme-iron-catalyzed metabolism with H2S. Angew. Chem. Int. Ed. 2013, 52, 1. (14) Hochlaf, M.; Linguerri, R.; Francisco, J. S. On the role of the simplest S-nitrosothiol, HSNO, in atmospheric and biological processes. J. Chem. Phys. 2013, 139, 234304. (15) Ivanova, L. V.; Anton, B. J.; Timerghazin, Q. K. On the possible biological relevance of HSNO isomers: a computational investigation. Phys. Chem. Chem. Phys. 2014, 16, 8476. (16) Nava, M.; Martin-Drumel, M.-A.; Lopez, C. A.; Crabtree, K. N.; Womack, C. C.; Nguyen, T. L.; Thorwirth, S.; Cummins, C. C.; Stanton, J. F.; McCarthy, M. C. Spontaneous and selective formation of HSNO, a crucial intermediate linking H2S and nitroso chemistries. J. Am. Chem. Soc. 2016, 138, 11441. (17) Cortese-Krott, M. M.; Fernandez, B.O.; Santos, J. L. T.; Mergia, E.; Grman, M.; Nagy, P.; Kelm, M.; Butler, A.; Feelisch, M. Nitrosopersulfide SSNO- accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide. Redox Biology 2014, 2, 234. (18) Cortese-Krott, M. M.; Kuhnle, G. G. C.; Dyson, A.; Fernandez, B. O.; Grman, M.; DuMond, J. F.; Barrow, M. P.; McLeod, G.; Nakagawa, H.; Ondrias, K.; et al. Key bioactive reaction

13



products of the NO/H2S interaction are S/N-hybrid species, polysulfides, and nitroxyl. Proc. Natl. Acad. Sci. USA 2015, 112, E4651. (19) Bianco, C. L.; Fukuto, J. M. Examining the reaction of NO and H2S and the possible cross-talk between the two signaling pathways. Proc. Natl. Acad. Sci. USA 2015, 112, 10573. (20) Marcolongo, J. P.; Morzan, U. N.; Zeida, A.; Scherlisa, D. A.; Olabe, J. A. Nitrosodisulfide [S2NO]- (perthionitrite) is a true intermediate during the "cross-talk'' of nitrosyl and sulfide. Phys. Chem. Chem. Phys. 2016, 18, 30047. (21) Gao, Y.; Toubaei, A.; Kong, X.; Wu, G. Solving the 170-year-old mystery about red-violet and blue transient Intermediates in the Gmelin reaction. Chemistry, 2015, 21, 17172. (22) Hartmann, N. J.; Wu, G.; Hayton, T. W. Reactivity of a nickel sulfide with carbon monoxide and nitric oxide. J. Am. Chem. Soc. 2016, 138, 12352. (23) Wedmann, R.; Zahl, A.; Shubina, T. E.; Dürr, M.; Heinemann, F. W.; Bugenhagen, B. E. C.; Burger, P.; Ivanovic-Burmazovic, I.; Filipovic, M. R. Does perthionitrite (SSNO-) account for sustained bioactivity of NO? A (bio)chemical characterization. Inorg. Chem. 2015, 54, 9367. (24) MOLPRO (version 2015) is a package of ab initio programs written by Werner, H.-J.; Knowles et al. (25) Ayari, T.; Jaidane, NE.; Mogren Al Mogren, M.; Francisco, J. S.; Hochlaf, M. Toward the laboratory identification of [O,N,S,S] isomers: Implications for biological NO chemistry J. Chem Phys. 2016, 144, 234316. (26) Knowles, P. J.; Hampel, C.; Werner, H.-J. Coupled-cluster theory for high-spin, open-shell reference wave-functions J. Chem. Phys. 1993, 99, 5219. (27) Knowles, P. J.; Hampel, C.; Werner, H.-J. Coupled cluster theory for high spin, open shell reference wave functions J. Chem. Phys. 2000, 112, 3106. (28) Werner, H. J.; Adler, T. B.; Manby, F. R. General orbital invariant MP2-F12 theory J. Chem. Phys. 2007, 126, 164102. (29) Adler, T. B.; Knizia, G.; Werner, H.-J. A simple and efficient CCSD(T)-F12 approximation J. Chem. Phys. 2007, 127, 221106. (30) Knizia, G.; Adler, T. B.; Werner, H.-J. Simplified CCSD(T)-F12 methods: Theory and benchmarks J. Chem. Phys. 2009, 130, 054104. (31) Knowles, P. J.; Werner, H.-J. An efficient 2nd-order MC SCF method for long configuration expansions. Chem. Phys. Lett. 1985, 115, 259. (32) Werner, H.-J.; Knowles, P. J. A 2nd order multiconfiguration SCF procedure with optimum convergence. J. Chem. Phys. 1985, 82, 5053. (33) Kendall, R. A.; Dunning, Jr. T. H.; Harrison, R. J. Electron-affinities of the 1st-row atoms revisited - systematic basis-sets and wave-functions J. Chem. Phys. 1992, 96, 6796.

14


Page 14 of 17

Page 15 of 17 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(34) Woon, D. E.; Dunning, Jr. T. H. Gaussian-basis sets for use in correlated molecular calculations.3. The atoms aluminum through argon J. Chem. Phys. 1993, 98, 1358. (35) Dunning, Jr. T. H.; Peterson, K. A.; Wilson, A. K. Gaussian basis sets for use in correlated molecular calculations. X. The atoms aluminum through argon revisited J. Chem. Phys. 2001, 114, 9244. (36) Ben Yaghlane, S.; Jaidane, N.-E.; Cotton, C. E.; Francisco, J. S.; Mogren Al Mogren, M.; Linguerri, R.; Hochlaf, M. Theoretical spectroscopic investigations of HNSq and HSNq (q=0,+1,-1) in the gas phase J. Chem. Phys. 2014, 140, 244309. (37) Ben Yaghlane, S.; Cotton, C. E.; Francisco, J. S.; Mogren Al Mogren, M.; Linguerri, R.; Hochlaf, M. Ab initio structural and spectroscopic study of HPSx and HSPx (x=0,+1,-1) in the gas phase J. Chem. Phys. 2013, 139, 174313. (38) Peterson, K. A.; Adler, T. B.; Werner, H.-J. Systematically convergent basis sets for explicitly correlated wavefunctions: The atoms H, He, B-Ne, and Al-Ar J. Chem. Phys. 2008, 128, 084102. (39) Helgaker, T.; Klopper, W.; Koch, H.; Noga, J. Basis-set convergence of correlated calculations on water J.Chem. Phys. 1997, 106, 9639. (40) Puzzarini, C. Extrapolation to the complete basis set limit of structural parameters: Comparison of different approaches. J. Phys. Chem. A 2009, 113, 14530–14535. (41) Werner, H.-J.; Knowles, P. J. An efficient internally contracted multiconfiguration reference configuration-interaction method J. Chem. Phys. 1988, 89, 5803. (42) Knowles, P. J.; Werner, H.-J. An efficient method for the evaluation of coupling-coefficients in configuration-interaction calculations Chem. Phys. Lett. 1988, 145, 514. (43) Shamasundar, K. R.; Knizia, G.; Werner, H.-J. A new internally contracted multi-reference configuration interaction method J. Chem. Phys. 2011, 135, 054101. (44) Shiozaki, T.; Knizia, G.; Werner, H.-J. Explicitly correlated multireference configuration interaction: MRCI-F12 J. Chem. Phys. 2011, 134, 034113. (45) Shiozaki, T.; Werner, H.-J. Explicitly correlated multireference configuration interaction with multiple reference functions: Avoided crossings and conical intersections J. Chem. Phys. 2011, 134, 184104. (46) Shiozaki, T.; Werner, H.-J. Multireference explicitly correlated F12 theories Mol. Phys. 2013, 111, 607. (47) Weaver, A.; Arnold, D.W.; Bradforth, S.E.; Neumark, D.M. Examination of the 2A′2 and 2E′ states of NO3 by ultraviolet photoelectron spectroscopy of NO3-. J. Chem. Phys. 1991, 94, 1740. (48) Senent, M. L.; Hochlaf, M. Reactivity of anions in interstellar media: Detectability and applications. Ap. J. 2013, 768, 59. (49) http://webbook.nist.gov 15



(50) Travers, M.J.; Cowles, D.C.; Ellison, G.B. Reinvestigation of the electron affinities of O2 and NO. Chem. Phys. Lett. 1989, 164, 449. (51) Timerghazin, Q. K.; Peslherbe, G. H.; English, A. M. Structure and stability of HSNO, the simplest S-nitrosothiol. Phys. Chem. Chem. Phys. 2008, 10, 1532. (52) Bailey, T. Spencer; Henthorn, H. A.; Pluth, M. D. The intersection of NO and H2S: Persulfides generate NO from nitrite through polysulfide formation. Inorg. Chem. 2016, 55, 12618. (53) Seel, F.; Kuhn, R.; Simon, G.; Wagner, M. PNP-perthionitrite and PNP-monothionitrite. Z. Naturforsch. B 1985, 40b, 1607. (54) Ejsing, A. M.; Nielsen, S. B. Computational study on the negative electron affinities of NO2.(H2O)n clusters (n=0-30). J. Chem. Phys. 2007, 126, 154313. (55) Wu Z.; Liu, Q.; Xu, J.; Sun, H.; Li, D.; Song, C.; M. Andrada, D.; Frenking, G.; Trabelsi, T.; Francisco, J S.; et al. Heterocumulene sulfinyl radical OCNSO. Angew. Chem. Int. Ed. Engl. 2017, 56, 2140.

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On the Identification of Key Intermediates During the NO and H2S

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